Advertisement

Acta Physiologiae Plantarum

, 37:203 | Cite as

Salt priming improved salt tolerance in sweet sorghum by enhancing osmotic resistance and reducing root Na+ uptake

  • Kun Yan
  • Hualing Xu
  • Wei Cao
  • Xiaobing Chen
Original Article

Abstract

This study attempted to explore how salt priming affected salt tolerance in sweet sorghum with emphasis on root Na+ uptake. After 10 days of pretreatment with 150 mM NaCl, plants were stressed with 300 mM NaCl. After salt stress for 7 days, dry matter of root and shoot decreased by 58.7 and 69.7 % in non-pretreated plants and by 37.9 and 41.3 % in pretreated plants. Consistently, pretreated plants maintained higher photosynthetic rate during salt stress, suggesting the enhanced tolerance by salt priming. Salt priming enhanced osmotic resistance, as proline and relative water contents in the leaf were higher in pretreated plants under salt stress. Salt priming alleviated salt-induced oxidative damage not by improving antioxidant protection due to lower increase in leaf malondialdehyde content and no extra induction on ascorbate peroxidase, catalase, superoxide dismutase, ascorbic acid and reduced glutathione in pretreated plants. After 7 days of salt stress, root Na+ efflux increased by 8.5- and 3.9-folds in pretreated and non-pretreated plants, suggesting that salt priming reduced root Na+ uptake, and then root and leaf Na+ accumulation were mitigated in pretreated plants. However, root Na+ extrusion became indifferent between pretreated and non-pretreated plants under salt stress after inhibiting plasma membrane (PM) Na+/H+ antiporter. Thus, the greater Na+ extrusion induced by salt priming had relation to PM Na+/H+ antiporter. Overall, salt priming improved salt tolerance in sweet sorghum by enhancing osmotic resistance and reducing root Na+ uptake.

Keywords

Antioxidant Osmotic adjustment Photosynthesis Root Na+ extrusion Salt pretreatment 

Abbreviations

APX

Ascorbate peroxidase

AsA

Ascorbic acid

CAT

Catalase

Ci

Intercellular CO2 concentration

gs

Stomatal conductance

Fv/Fm

The maximum photochemical efficiency of PSII

GSH

Glutathione

MDA

Malondialdehyde

NMT

Non-invasive micro-test technique

Pn

Photosynthetic rate

PM

Plasma membrane

PSII

Photosystem II

ROS

Reactive oxygen species

SOD

Superoxide dismutase

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (41201292).

References

  1. Abbas T, Balal RM, Shahid MA, Pervez MA, Ayyub CM, Aqueel MA, Javaid MM (2015) Silicon-induced alleviation of NaCl toxicity in okra (Abelmoschus esculentus) is associated with enhanced photosynthesis, osmoprotectants and antioxidant metabolism. Acta Physiol Plant 37:6. doi: 10.1007/s11738-014-1768-5 CrossRefGoogle Scholar
  2. Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056. doi: 10.1104/pp.123.3.1047 PubMedCentralCrossRefPubMedGoogle Scholar
  3. Almodares A, Hadi MR, Ahmadpour H (2008) Sorghum stem yield and soluble carbohydrates under different salinity levels. Afr J Biotechnol 7:4051–4055Google Scholar
  4. Almodares A, Hadi MR, Kholdebarin B, Samedani B, Kharazian ZA (2014) The response of sweet sorghum cultivars to salt stress and accumulation of Na+, Cl and K+ ions in relation to salinity. J Environ Biol 35(4):733–799PubMedGoogle Scholar
  5. Amzallag GN, Lerner HR, Poljakoffmayber A (1990) Induction of increased salt tolerance in sorghum-bicolor by NaCl pretreatment. J Exp Bot 41:29–34. doi: 10.1093/Jxb/41.1.29 CrossRefGoogle Scholar
  6. Aparicio C, Urrestarazu M, Cordovilla MD (2014) Comparative physiological analysis of salinity effects in six olive genotypes. HortScience 49:901–904Google Scholar
  7. Arnon DI (1950) Dennis Robert Hoagland: 1884-1949. Science 112(2921):739–742. doi: 10.1126/science.112.2921.739 CrossRefPubMedGoogle Scholar
  8. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216. doi: 10.1016/j.envexpbot.2005.12.006 CrossRefGoogle Scholar
  9. Ashrafi E, Razmjoo J, Zahedi M, Pessarakli M (2015) Screening alfalfa for salt tolerance based on lipid peroxidation and antioxidant enzymes. Agron J 107(1):167–173. doi: 10.2134/agronj14.0248 CrossRefGoogle Scholar
  10. Azzabi G, Pinnola A, Betterle N, Bassi R, Alboresi A (2012) Enhancement of non-photochemical quenching in the bryophyte Physcomitrella patens during acclimation to salt and osmotic stress. Plant Cell Physiol 53(10):1815–1825. doi: 10.1093/pcp/pcs124 CrossRefPubMedGoogle Scholar
  11. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194. doi: 10.1093/aob/mcf118 PubMedCentralCrossRefPubMedGoogle Scholar
  12. Bojorquez-Quintal E, Velarde-Buendia A, Ku-Gonzalez A, Carillo-Pech M, Ortega-Camacho D, EchevarrIa-Machado I, Pottosin I, Martinez-Estevez M (2014) Mechanisms of salt tolerance in habanero pepper plants (Capsicum chinense Jacq.): proline accumulation, ions dynamics and sodium root-shoot partition and compartmentation. Front Plant Sci 5:1–4. doi: 10.3389/fpls.2014.00605 Google Scholar
  13. Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 155(3):481–494. doi: 10.1093/aob/mcu219 CrossRefGoogle Scholar
  14. Brestic M, Zivcak M, Kalaji HM, Carpentier R, Allakhverdiev SI (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105. doi: 10.1016/j.plaphy.2012.05.012 CrossRefPubMedGoogle Scholar
  15. Chao DY, Dilkes B, Luo HB, Douglas A, Yakubova E, Lahner B, Salt DE (2013) Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341:658–659. doi: 10.1126/science.1240561 PubMedCentralCrossRefPubMedGoogle Scholar
  16. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. doi: 10.1093/Aob/Mcn125 PubMedCentralCrossRefPubMedGoogle Scholar
  17. Chen P, Yan K, Shao H, Zhao S (2013) Physiological mechanisms for high salt tolerance in wild soybean (Glycine soja) from yellow river delta, China: photosynthesis, osmotic regulation, ion flux and antioxidant capacity. PLoS ONE 8:e83227. doi: 10.1371/journal.pone.0083227 PubMedCentralCrossRefPubMedGoogle Scholar
  18. Davila-Gomez FJ, Chuck-Hernandez C, Perez-Carrillo E, Rooney WL, Serna-Saldivar SO (2011) Evaluation of bioethanol production from five different varieties of sweet and forage sorghums (Sorghum bicolor (L) Moench). Ind Crop Prod 33:611–616. doi: 10.1016/j.indcrop.2010.12.022 CrossRefGoogle Scholar
  19. Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U (2006) Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil 284:363–373. doi: 10.1007/s11104-006-0043-y CrossRefGoogle Scholar
  20. Hussain S, Luro F, Costantino G, Ollitrault P, Morillon R (2012) Physiological analysis of salt stress behaviour of citrus species and genera: low chloride accumulation as an indicator of salt tolerance. South Afr J Bot 81:103–112. doi: 10.1016/j.sajb.2012.06.004 CrossRefGoogle Scholar
  21. Jabeen Z, Hussain N, Han Y, Shah MJ, Zeng F, Zeng J, Zhang G (2014) The differences in physiological responses, ultrastructure changes, and Na+ subcellular distribution under salt stress among the barley genotypes differing in salt tolerance. Acta Physiol Plant 36:2397–2407. doi: 10.1007/s11738-014-1613-x CrossRefGoogle Scholar
  22. Jabeen Z, Hussain N, Wu D, Han Y, Shamsi I, Wu F, Zhang G (2015) Difference in physiological and biochemical responses to salt stress between Tibetan wild and cultivated barleys. Acta Physiol Plant 37:180. doi: 10.1007/s11738-015-1920-x CrossRefGoogle Scholar
  23. Kalaji HM, Govindjee Bosa K, Koscielniakd J, Zuk-Golaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72. doi: 10.1016/j.envexpbot.2010.10.009 CrossRefGoogle Scholar
  24. Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allakhverdiev SI, Goltsev V (2014a) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Biochem 81:16–25. doi: 10.1016/j.plaphy.2014.03.029 CrossRefPubMedGoogle Scholar
  25. Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dabrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serodio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014b) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158. doi: 10.1007/s11120-014-0024-6 PubMedCentralCrossRefPubMedGoogle Scholar
  26. Kiani-Pouya A (2015) Changes in activities of antioxidant enzymes and photosynthetic attributes in triticale (×Triticosecale Wittmack) genotypes in response to long-term salt stress at two distinct growth stages. Acta Physiol Plant 37:72. doi: 10.1007/s11738-015-1819-6 CrossRefGoogle Scholar
  27. Kong XQ, Luo Z, Dong HH, Eneji AE, Li WJ (2012) Effects of non-uniform root zone salinity on water use, Na+ recirculation, and Na+ and H+ flux in cotton. J Exp Bot 63:2105–2116. doi: 10.1093/Jxb/Err420 PubMedCentralCrossRefPubMedGoogle Scholar
  28. Lu KX, Yang Y, He Y, Jiang DA (2008) Induction of cyclic electron flow around photosystem 1 and state transition are correlated with salt tolerance in soybean. Photosynthetica 46:10–16. doi: 10.1007/s11099-008-0003-2 CrossRefGoogle Scholar
  29. Maathuis FJM, Ahmad I, Patishtan J (2014) Regulation of Na+ fluxes in plants. Front Plant Sci 5:467. doi: 10.3389/fpls.2014.00467 PubMedCentralCrossRefPubMedGoogle Scholar
  30. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. doi: 10.1016/S1360-1385(02)02312-9 CrossRefPubMedGoogle Scholar
  31. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250. doi: 10.1046/j.0016-8025.2001.00808.x CrossRefPubMedGoogle Scholar
  32. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi: 10.1146/annurev.arplant.59.032607.092911 CrossRefPubMedGoogle Scholar
  33. Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043. doi: 10.1093/Jxb/Erj100 CrossRefPubMedGoogle Scholar
  34. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421. doi: 10.1016/j.bbabio.2006.11.019 CrossRefPubMedGoogle Scholar
  35. Murtaza G, Ghafoor A, Owens G, Qadir M, Kahlon UZ (2009) Environmental and economic benefits of saline-sodic soil reclamation using low-quality water and soil amendments in conjunction with a rice-wheat cropping system. J Agron Crop Sci 195:124–136. doi: 10.1111/j.1439-037X.2008.00350.x CrossRefGoogle Scholar
  36. Neto ADD, Prisco JT, Eneas J, de Abreu CEB, Gomes E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94. doi: 10.1016/j.envexpbot.2005.01.008 CrossRefGoogle Scholar
  37. Oukarroum A, Bussotti F, Goltsev V, Kalaji HM (2015) Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. Environ Exp Bot 109:80–88. doi: 10.1016/j.envexpbot.2014.08.005 CrossRefGoogle Scholar
  38. Rozema J, Flowers T (2008) Ecology crops for a salinized world. Science 322:1478–1480. doi: 10.1126/science.1168572 CrossRefPubMedGoogle Scholar
  39. Saha P, Chatterjee P, Biswas AK (2010) NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata L. Wilczek). Indian J Exp Biol 48:593–600PubMedGoogle Scholar
  40. Saha P, Kunda P, Biswas AK (2012) Influence of sodium chloride on the regulation of Krebs cycle intermediates and enzymes of respiratory chain in mungbean (Vigna radiata L. Wilczek) seedlings. Plant Physiol Biochem 60:214–222. doi: 10.1016/j.plaphy.2012.08.008 CrossRefPubMedGoogle Scholar
  41. Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49:85–91. doi: 10.1007/s10535-005-5091-2 CrossRefGoogle Scholar
  42. Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66. doi: 10.1038/Nature11909 PubMedCentralCrossRefPubMedGoogle Scholar
  43. Shao Y, Gao J, Wu X, Li Q, Wang J, Ding P, Lai X (2015) Effect of salt treatment on growth, isoenzymes and metabolites of Andrographis paniculata (Burm. f.) Nees. Acta Physiol Plant 37:35. doi: 10.1007/s11738-015-1787-x CrossRefGoogle Scholar
  44. Sivritepe N, Sivritepe H, Turkan I, Bor M, Ozdemir F (2008) NaCl pre-treatments mediate salt adaptation in melon plants through antioxidative system. Seed Sci Technol 36:360–370CrossRefGoogle Scholar
  45. Song J, Shi GW, Gao B, Fan H, Wang BS (2011) Waterlogging and salinity effects on two Suaeda salsa populations. Physiol Plant 141:343–351. doi: 10.1111/j.1399-3054.2011.01445.x CrossRefPubMedGoogle Scholar
  46. Sun J, Chen SL, Dai SX, Wang RG, Li NY, Shen X, Zhou XY, Lu CF, Zheng XJ, Hu ZM, Zhang ZK, Song J, Xu Y (2009) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol 149:1141–1153. doi: 10.1104/pp.108.129494 PubMedCentralCrossRefPubMedGoogle Scholar
  47. Tajdoost S, Farboodnia T, Heidari R (2007) Salt pretreatment enhance salt tolerance in Zea mays L. seedlings. Pak J Biol Sci 10:2086–2090CrossRefPubMedGoogle Scholar
  48. Tanou G, Fotopoulos V, Molassiotis A (2012) Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front Plant Sci 3:216. doi: 10.3389/fpls.2012.00216 PubMedCentralCrossRefPubMedGoogle Scholar
  49. Tari I, Laskay G, Takacs Z, Poor P (2013) Response of sorghum to abiotic stresses: a review. J Agron Crop Sci 199:264–274. doi: 10.1111/jac.12017 CrossRefGoogle Scholar
  50. Umezawa T, Shimizu K, Kato M, Ueda T (2000) Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiol Plant 110:59–63. doi: 10.1034/j.1399-3054.2000.110108.x CrossRefGoogle Scholar
  51. Vasilakoglou I, Dhima K, Karagiannidis N, Gatsis T (2011) Sweet sorghum productivity for biofuels under increased soil salinity and reduced irrigation. Field Crop Res 120:38–46. doi: 10.1016/j.fcr.2010.08.011 CrossRefGoogle Scholar
  52. Yan K, Chen W, He XY, Zhang GY, Xu S, Wang LL (2010) Responses of photosynthesis, lipid peroxidation and antioxidant system in leaves of Quercus mongolica to elevated O3. Environ Exp Bot 69:198–204. doi: 10.1016/j.envexpbot.2010.03.008 CrossRefGoogle Scholar
  53. Yan K, Chen P, Shao H, Zhao S, Zhang L, Zhang L, Xu G, Sun J (2012) Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum. J Agron Crop Sci 198:218–226. doi: 10.1111/j.1439-037X.2011.00498.x CrossRefGoogle Scholar
  54. Yan K, Shao HB, Shao CY, Chen P, Zhao SJ, Brestic M, Chen XB (2013) Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 35:2867–2878. doi: 10.1007/s11738-013-1325-7 CrossRefGoogle Scholar
  55. Yan K, Wu CW, Zhang LH, Chen XB (2015) Contrasting photosynthesis and photoinhibition in tetraploid and its autodiploid honeysuckle (Lonicera japonica Thunb.) under salt stress. Front Plant Sci 6:227. doi: 10.3389/fpls.2015.00227 Google Scholar
  56. Yazici I, Tuerkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57. doi: 10.1016/j.envexpbot.2007.02.010 CrossRefGoogle Scholar
  57. Zhang L, Ma H, Chen T, Pen J, Yu S, Zhao X (2014) Morphological and physiological responses of cotton (Gossypium hirsutum L.) plants to salinity. PLoS ONE 9(11):e112807. doi: 10.1371/journal.pone.0112807 PubMedCentralCrossRefPubMedGoogle Scholar
  58. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445. doi: 10.1016/S1369-5266(03)00085-2 CrossRefPubMedGoogle Scholar
  59. Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang XH, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosyn Res 117:529–546. doi: 10.1007/s11120-013-9885-3 CrossRefPubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2015

Authors and Affiliations

  1. 1.Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences (CAS)YantaiChina
  2. 2.Shandong Provincial Key Laboratory of Coastal Environmental Processes, YICCASYantaiChina
  3. 3.Dongying Academy of Agricultural SciencesDongyingChina
  4. 4.Bureau of Education and SportYantaiChina

Personalised recommendations